Levelling-up rhodolith-bed science to address global-scale conservation challenges.

Global marine conservation remains fractured by an imbalance in research efforts and policy actions, limiting progression towards sustainability. Rhodolith beds represent a prime example, as they have ecological importance on a global scale, provide a wealth of ecosystem functions and services, including biodiversity provision and potential climate change mitigation, but remain disproportionately understudied, compared to other coastal ecosystems (tropical coral reefs, kelp forests, mangroves, seagrasses). Although rhodolith beds have gained some recognition, as important and sensitive habitats at national/regional levels during the last decade, there is still a notable lack of information and, consequently, specific conservation efforts. We argue that the lack of information about these habitats, and the significant ecosystem services they provide, is hindering the development of effective conservation measures and limiting wider marine conservation success. This is becoming a pressing issue, considering the multiple severe pressures and threats these habitats are exposed to (e.g., pollution, fishing activities, climate change), which may lead to an erosion of their ecological function and ecosystem services. By synthesizing the current knowledge, we provide arguments to highlight the importance and urgency of levelling-up research efforts focused on rhodolith beds, combating rhodolith bed degradation and avoiding the loss of associated biodiversity, thus ensuring the sustainability of future conservation programs.

Diversidad de los hábitats submareales de la Península de Santa Elena e Islas Murciélago, Pacífico Norte, Costa Rica

Introducción: Los hábitats costeros de todo el mundo están experimentando una presión cada vez mayor debido a la contaminación, el desarrollo costero, la pesca y el cambio climático. Identificar y registrar la biodiversidad costera es esencial para evaluar la salud, los cambios y el alcance de la pérdida de biodiversidad de los ecosistemas. Los hábitats costeros tropicales como los arrecifes de coral y los lechos de pastos marinos han sido el foco de investigación de los científicos durante las últimas décadas; sin embargo, se han descuidado otros ecosistemas, como los bosques de macroalgas, los fondos de sedimentos submareales (20-30 m de profundidad) y los arrecifes rocosos. Objetivo: Este trabajo reporta la biodiversidad marina asociada con arrecifes rocosos, arrecifes de coral, bosques de Sargazo y fondos submareales sedimentarios (20-30 m de profundidad), en un área tropical de afloramiento estacional (Península de Santa Elena, Bahía de Santa Elena e Islas Murciélago, Costa Rica). Métodos: Durante la Expedición Santa Elena (21 de abril-2 de mayo de 2018), se visitaron un total de 28 sitios para registrar la biodiversidad en cuatro hábitats diferentes (arrecifes rocosos y de coral, bosques de sargazo y fondos de sedimentos submareales), utilizando SCUBA, en muestreos sistemáticos, evaluaciones visuales y en algunos fondos de sedimentos se utilizó una draga de arrastre por 20 minutos. Resultados: Se identificaron un total de 254 taxones, siendo los peces óseos el grupo más diverso con 91 especies, seguido de los gasterópodos (25 spp.), las algas rojas (21 spp.) y los antozoos (19 spp.). Se reportan cuatro nuevos registros para el Pacífico continental de Costa Rica, incluida la subclase de una anémona tubícola (Ceriantharia). Conclusiones: Los resultados muestran que la península de Santa Elena, la bahía de Santa Elena y las islas Murciélago albergan hábitats poco comunes y no estudiados, como bosques del alga parda Sargassum, fondos de sedimentos, arrecifes construidos por el coral masivo Pavona gigantea, que es muy inusual, y comunidades de arrecifes rocosos dominadas por colonias calcáreas de poliquetos (Salmacina tribranchiata).

Introduction: Worldwide, coastal habitats are experiencing increasing pressure from pollution, coastal development, fisheries, and climate change. Identifying and recording coastal biodiversity is essential to assess ecosystem health, changes and the extent of biodiversity loss. Coastal tropical habitats such as coral reefs and seagrass beds have been the research focus for scientists during the last decades; however, other ecosystems have been neglected, such as macroalgae forests, subtidal (20-30 m deep) sedimentary bottoms, and rocky reefs. Objective: Our study reports the marine biodiversity associated with rocky reefs, coral reefs, Sargassum forests and sedimentary subtidal bottoms (20-30 m deep), in a tropical seasonal upwelling area (Santa Elena Peninsula, Santa Elena Bay, and Murciélago Islands, Costa Rica). Methods: During the 'Santa Elena Expedition' (April 21-May 2 2018), a total of 28 sites were visited in order to record the biodiversity across four different habitats (rocky and coral reefs, Sargassum forests, subtidal sedimentary bottoms), using SCUBA and both systematic surveys and visual assessments; in some sedimentary bottoms a 20-minute dredge tows were done. Results: A total of 254 taxa were identified, being bony fishes the most diverse group (91 species), followed by gastropods (25 spp.), red algae (21 spp.) and anthozoans (19 spp.). We report four new records for the Pacific mainland of Costa Rica, including the subclass of tube-dwelling sea anemone (Ceriantharia). Conclusions: Our results show that Santa Elena Peninsula, Santa Elena Bay, and Murciélago Islands harbor uncommon and unstudied habitats, such as Sargassum forests, sedimentary bottoms, reefs constructed by the stony coral Pavona gigantea -which is very unusual- and rocky reef communities dominated by calcareous colonies of polychaetes (Salmacina tribranchiata).

Impact of El Niño 2015-2016 on the coral reefs of the Pacific of Costa Rica: the potential role of marine protection

Introduction: El Niño 2015-2016 was considered one of the most severe worldwide, causing the third global event of coral bleaching. Previous high-intensity El Niño events (1982-83 and 1997-98) caused high coral mortalities and deterioration of coral reef structures along the Eastern Tropical Pacific, affecting both ecosystem and associated economical activities. Objective: The aim of this study was to determine the impact of the most recent El Niño event on coral reefs from Cocos Island and the Pacific coast of southern Costa Rica. Methods: Coral reefs were surveyed before (2013-2014) and after (2016) the disturbance, using underwater visual censuses within belt transects, to quantify the bottom coverage at different depths. Results: In general, average live coral cover decreased 50% after the 2015-2016 El Niño event, with Golfo Dulce being the most affected area with 75% of live coral cover decline. However, in certain localities such as Isla del Coco and Isla del Caño, the effects of El Niño were apparently minimal, since no substantial loss of live coral cover was detected. Differences in the level of deterioration found between coral reefs could be related to several factors, including the age of the protected area, the distance to centers of human population, and the effectiveness in the application of management strategies. Conclusions: The synergistic impact of the 2015-16 El Niño event and other stressors (e.g. illegal fishing and unregulated coastal human development) increased the levels of disturbance on coral reefs, threatening their structure and functioning. It is necessary to strengthen conservation strategies in order to improve the resilience of coral reefs to the impact of natural and anthropogenic disturbances. Concrete actions such as coral reef restoration, marine environmental education, and marine spatial planning must become important tools to maintain the good health of coral reefs and ensure the sustainability of the goods and services provided by these ecosystems.

Introducción: El fenómeno El Niño del 2015-2016 fue considerado como uno de los más severos a nivel mundial, causando el tercer evento global de blanqueamiento coralino. Eventos previos de alta intensidad (1982-83 y 1997-98), causaron altas mortalidades coralinas y el deterioro de estructuras arrecifales a lo largo de Pacífico Tropical Oriental, afectando tanto al ecosistema como las actividades económicas asociadas. Objetivo: El objetivo de este estudio, fue determinar el impacto del evento El Niño 2015-2016 en la salud de los arrecifes coralinos de la Isla del Coco y la costa Pacífico Sur de Costa Rica. Métodos: La evaluación de los arrecifes de coral se realizó antes (2013-2014) y después (2016) de la perturbación, utilizando censos visuales subacuáticos en transectos de banda, con el fin de cuantificar la cobertura del fondo a distintas profundidades. Resultados: En general, la cobertura coralina viva promedio disminuyó 50% después del evento El Niño 2015-2016, siendo Golfo Dulce la zona más afectada con una reducción del 75%. Sin embargo, en ciertas localidades como las islas Coco y Caño, los efectos de El Niño fueron aparentemente mínimos, ya que no se detectó una pérdida sustancial de la cobertura coralina viva. Las diferencias en el nivel de deterioro encontradas entre los arrecifes podrían estar relacionadas con varios factores, incluyendo el tiempo transcurrido desde que se estableció el área protegida, la distancia a los centros de la población humana y la efectividad en la aplicación de estrategias de manejo. Conclusiones: El impacto sinérgico del evento El Niño 2015-2016 y otros factores de estrés (por ejemplo, la pesca ilegal y el desarrollo costero no regulado) incrementó los niveles de perturbación en los arrecifes coralinos, amenazando su estructura y funcionamiento. Es necesario fortalecer las estrategias de conservación para mejorar la resiliencia de los arrecifes coralinos ante el impacto de perturbaciones naturales y antropogénicas. Acciones concretas como la jardinería de corales, la educación ambiental marina y el ordenamiento espacial marino, deben convertirse en herramientas importantes para mantener la buena salud de los arrecifes coralinos y asegurar la sostenibilidad de los bienes y servicios proporcionados por estos ecosistemas.

The systematics of Lobophora (Dictyotales, Phaeophyceae) in the western Atlantic and eastern Pacific oceans: eight new species.

Lobophora is a common tropical to temperate genus of brown algae found in a plethora of habitats including shallow and deep-water coral reefs, rocky shores, mangroves, seagrass beds, and rhodoliths beds. Recent molecular studies have revealed that Lobophora species diversity has been severely underestimated. Current estimates of the species numbers range from 100 to 140 species with a suggested center of diversity in the Central Indo-Pacific. This study used three molecular markers (cox3, rbcL, psbA), different single-marker species delimitation methods (GMYC, ABGD, PTP), and morphological evidence to evaluate Lobophora species diversity in the Western Atlantic and the Eastern Pacific oceans. Cox3 provided the greatest number of primary species hypotheses(PSH), followed by rbcL and then psbA. GMYC species delimitation analysis was the most conservative across all three markers, followed by PTP, and then ABGD. The most informative diagnostic morphological characters were thallus thickness and number of cell layers in both the medulla and the dorsal/ventral cortices. Following a consensus approach, 14 distinct Lobophora species were identified in the Western Atlantic and five in the Eastern Pacific. Eight new species from these two oceans were herein described: L. adpressa sp. nov., L. cocoensis sp. nov., L. colombiana sp. nov., L. crispata sp. nov., L. delicata sp. nov., L. dispersa sp. nov., L. panamensis sp. nov., and L. tortugensis sp. nov. This study showed that the best approach to confidently identify Lobophora species is to analyze DNA sequences (preferably cox3 and rbcL) followed by comparative morphological and geographical assessment.

Chloroplast genomes as a tool to resolve red algal phylogenies: a case study in the Nemaliales.

BACKGROUND: Obtaining strongly supported phylogenies that permit confident taxonomic and evolutionary interpretations has been a challenge in algal biology. High-throughput sequencing has improved the capacity to generate data and yields more informative datasets. We sequenced and analysed the chloroplast genomes of 22 species of the order Nemaliales as a case study in the use of phylogenomics as an approach to achieve well-supported phylogenies of red algae. RESULTS: Chloroplast genomes of the order Nemaliales are highly conserved, gene-dense and completely syntenic with very few cases of gene loss. Our ML estimation based on 195 genes recovered a completely supported phylogeny, permitting re-classification of the order at various taxonomic levels. Six families are recognised and the placement of several previously contradictory clades is resolved. Two new sub-orders are described, Galaxaurineae and Nemaliineae, based on the early-branching nature and monophyly of the groups, and presence or absence of a pericarp. Analyses of subsets of the data showed that >90 % bootstrap support can be achieved with datasets as small as 2500 nt and that fast and medium evolving genes perform much better when it comes to resolving phylogenetic relationships. CONCLUSIONS: In this study we show that phylogenomics is an efficient and effective approach to investigate phylogenetic relationships. The six currently circumscribed Nemaliales families are clustered into two evolutionary lineages with strong statistical support based on chloroplast phylogenomic analyses. The conserved nature of red algal chloroplast genomes is a convenient and accessible source of data to resolve their ancient relationships.

Ecosistemas coralinos del Área de Conservación Osa, Costa Rica: estructura y necesidades de conservación / Osa Conservation Area (Costa Rica) coral ecosystems: structure and conservation needs

Resumen Costa Rica es considerado uno de los 20 países del mundo con mayor biodiversidad, entre los que destacan sus ecosistemas arrecifales. Más precisamente, el Pacífico Sur, el Área de Conservación Osa, se ha considerado como una de las zonas más diversas en estos ecosistemas. Estos arrecifes han sido estudiados desde inicios de los años 80's, pero enfocándose solamente en la cobertura coralinos de estos arrecifes. Por lo tanto, la presente investigación busca realizar una evaluación actualizada y con una metodología estándar él estado de varios componentes de los sistemas arrecifales de esta región. Entre el 2013 y el 2014, se visitaron cinco localidades: Dominicalito, Parque Nacional Marino Ballena, Reserva Biológica Isla del Caño, Península de Osa y Golfo Dulce, donde se evaluaron 27 sitios. En ellos se realizó la evaluación, a dos profundidades, de: cobertura del fondo, rugosidad del arrecife, diversidad y densidad de macroinvertebrados, así como la diversidad y biomasa de peces arrecifales. En términos generales los arrecifes de ACOSA, son moderadamente complejos y en ellos predominan el tapete algal (62.7%), mientras que la cobertura de coral vivo es moderada (16.5%). Se observó una diferencia entre la cobertura de tipos de sustratos por localidad, la cual puede estar atribuida a condiciones ambientales adversas (i.e. sedimentación, contaminación) para su desarrollo. Sin embargo, los arrecifes coralinos de Golfo Dulce e Isla del Caño muestran una notable recuperación al compararla con estudios previos. Se observaron 35 taxa de macroinvertebrados en los sitios estudiados, en su mayoría (58%) fueron poco abundantes u ocasionales. La mayor diversidad y densidad de macroinvertebrados se observó en Golfo Dulce y se determinaron diferencias significativas entre localidades. Este estudio brinda una línea base para muchos de estos organismos en varios de los sitios. Los equinoideos Diadema mexicanum y Eucidaris thouarsii fueron los organismos predominantes, y se reporta el cambute (Lobatus galeatus) en varios de los sitios de muestreo. De las 90 especies de peces, 10 fueron las de mayor ocurrencia y densidad. No hubo diferencias significativas en la diversidad y riqueza de especies de peces observadas entre localidades, pero si en la biomasa y en la composición de la comunidad íctica entre los sitios. Los sitios de la Isla del Caño fueron los más diversos de toda ACOSA, presentan biomasas importantes y de niveles tróficos altos. Mientras que Golfo Dulce difirió con respecto a las demás localidades. Según los resultados observados, los arrecifes de ACOSA presentan una alta biodiversidad. Las condiciones del de los ecosistemas indican que más esfuerzos de conservación, uso sostenible y manejo efectivo de loa recursos en tierra como en el mar deben ser implementados. El monitoreo ecológico va a proveer de la información sobre las tendencias y las relaciones entre el estado de los ecosistemas arrecifales y las condiciones ambientales.

Abstract Costa Rica is considered one of the 20 most biodiverse countries in the world, which includes it´s well known reefs ecosystems. Specifically, the South Pacific region, the Osa Conservation Area (ACOSA), holds one of the richest reefs of the country. Even though many of these reefs have been studied since the 1980´s, most of them had focused mainly on coral cover condition. Therefore, the present research aims to complete and update an evaluation of the main biological components of ACOSA´s reefs ecosystems, using a standard methodology. Between 2013 and 2014, five localities were visited: Dominicalito, Marino Ballena National Park, Caño Island Biological Reserve, Osa Peninsula and Golfo Dulce, on which 27 sites were evaluated. Transects at two depths in each site were done to estimate substrate cover, reef rugosity, macroinvertebrates diversity and density, and reef fishes composition and biomass. Results indicate that ACOSA´s reef are moderately complex and on most of them the substrate is dominated by turf (62.7%) and live coral cover is moderate (16.5%). Substrate cover was significantly different between localities, which can be attributed to adverse environmental conditions for reef development (e.g. sedimentation, pollution). However, reefs in Golfo Dulce and Caño Island BR showed a significant coral cover recovery since last studied. Of 35 taxa of macroinvertebrates identified, 58% had low abundance or were observed occasionally. Golfo Dulce presented the highest diversity and density of macroinvertebrates and significant differences were observed between localities. On this group, this study is providing an information baseline of most sites analyzed. The echinoids Diadema mexicanum and Eucidaris thouarsii were the most abundant and the conch (Lobatus galeatus) was reported for many of the sites. Of the 90 species of reef fishes documented, ten were common and with the highest densities. There were no significant differences in the diversity and richness of the reef fishes between localities, but fishes' biomass and composition of fish community were different between sites. Caño Island´s sites were the most diverse of ACOSA, and presented the highest biomass and trophic levels of the region. Golfo Dulce´s reef fish composition differs from the other localities. According to the results, ACOSA´s reef ecosystems have a high biodiversity. The ecosystems conditions observed indicate that more conservation efforts, sustainable use and effective management of land and marine resources should be implemented. Ecological monitoring will provide the information about trends and the relationship between reef ecosystems state and environmental conditions. Rev. Biol. Trop. 63 (Suppl. 1): 219-259. Epub 2015 April 01.

Species Diversity, Phylogeny and Large Scale Biogeographic Patterns of the Genus Padina (Phaeophyceae, Dictyotales).

The brown algal genus Padina (Dictyotales, Phaeophyceae) is distributed worldwide in tropical and temperate seas. Global species diversity and distribution ranges, however, remain largely unknown. Species-level diversity was reassessed using DNA-based, algorithmic species delineation techniques based on cox3 and rbcL sequence data from 221 specimens collected worldwide. This resulted in estimates ranging from 39 to 61 putative species (ESUs), depending on the technique as well as the locus. We discuss the merits, potential pitfalls, and evolutionary and biogeographic significance of algorithmic species delineation. We unveil patterns whereby ESUs are in all but one case restricted to either the Atlantic or Indo-Pacific Ocean. Within ocean basins we find evidence for the vast majority of ESUs to be confined to a single marine realm. Exceptions, whereby ESUs span up to three realms, are located in the Indo-Pacific Ocean. Patterns of range-restricted species likely arise by repeated founder events and subsequent peripatric speciation, hypothesized to dominate speciation mechanisms for coastal marine organisms in the Indo-Pacific. Using a three-gene (cox3, psaA and rbcL), relaxed molecular clock phylogenetic analysis we estimated divergence times, providing a historical framework to interpret biogeographic patterns.

Physical factors contributing to the benthic dominance of the alga Caulerpa sertularioides (Caulerpaceae, Chlorophyta) in the upwelling Bahía Culebra, north Pacific of Costa Rica / Factores físicos que contribuyen a la dominancia bentónica del alga Caulerpa sertularioides (Caulerpaceae, Chlorophyta) en la surgencia Bahía Culebra, Pacífico norte de Costa Rica

Caulerpa sertularioides has been spreading in Bahía Culebra, a seasonal upwelling bay in the north Pacific of Costa Rica, since 2001. The survey was carried out from December 2003 to March 2005, in several locations around Bahía Culebra, located inside the Gulf of Papagayo. This study investigated spatial and temporal patterns, percent coverage, monthly growth rate, reproductive adaptations, and morphological variations of frond length and stolon diameter of Caulerpa sertularioides, at different environmental physical and chemical factors at the bay. The alga extended to depths of 23 m on a variety of substrates. The stolons extended quickly, with a maximum growth rate of 31.2 cm month-1. This alga grows mainly by fragmentation of its fronds and stolons; nevertheless it can also reproduce sexually by releasing gametes in the water column. These two modes of spreading promote the adaptation of this opportunistic species to environmental, chemical, and physical changes at this bay. At the same time the alga showed variations in the length of its fronds and stolons, adapting to conditions such as depth and season. Average percent cover and frond density increased during the dry season when the upwelling of nutrients and cold water occurs. In the rainy season the average percent cover and frond density decreased; however there was a peak in September, when high precipitation resulted in runoff into the bay of nutrient-rich waters. The morphological and physiological plasticity of C. sertularioides, in synergy with its predominant clonal propagation and sexual reproduction provided this species with a great adaptability to changes in temperature and nutrient concentration at Bahía Culebra.

Desde el 2001 se ha observado una propagación del alga verde Caulerpa sertularioides en Bahía Culebra, zona de afloramiento costero, en el Pacífico norte de Costa Rica. El muestreo se llevó acabo entre Diciembre 2003 a marzo 2005, en varias localidades de Bahía Culebra. En este estudio se presentan los patrones de distribución, cobertura, tasa mensual de crecimiento, adaptaciones reproductivas y variaciones morfológicas del largo de la fronda y diámetro del estolón de Caulerpa sertularioides, a diferentes factores ambientales físico-químicos en Bahía Culebra. Esta alga se extiende hasta profundidades de 23 m, en una gran variedad de sustratos. Los estolones se extienden rápidamente, con un crecimiento máximo de 31.2 cm mes-1. Esta alga se propaga principalmente por la fragmentación de sus frondas y estolones, así mismo se reproduce sexualmente liberando gametos a la columna de agua. Estos modos de reproducción promueven la adaptación de esta especie oportunista, a los cambios ambientales, tanto químicos, como físicos, de la bahía. Al mismo tiempo esta alga presenta variaciones en el largo de sus frondas y el diámetro del rizoma, adaptándose a diferentes profundidades y condiciones de la época del año. El porcentaje de cobertura y densidad de frondas aumentan durante la época seca, cuando emergen aguas frías y nutrientes por el afloramiento costero. Por otro lado, en la época lluviosa estas medidas decrecen, sin embargo se presenta un pico en setiembre, cuando la precipitación aumenta y llega una carga extra de nutrientes a la bahía por escorrentía. La plasticidad morfológica y fisiológica de C. sertularioides, en sinergia con su propagación clonal, proveen a esta alga con una gran adaptabilidad a los cambios en temperatura y nutrientes de Bahía Culebra.